Use of immunoglobulins in the prevention of GvHD in a xenogeneic NOD/SCID/γc- mouse model

Bone Marrow Transplantation

Volumn 47, Issue 3, 2012, Pages 439-450

  Gregoire Gauthier, J ^a   Durrieu, L ^a   Duval, A ^a   Fontaine, F ^a   Dieng, M M ^a   Bourgey, M ^a   Patey Mariaud De Serre, N ^a   Louis, I ^a,b   Haddad, E ^a,b  

^a UNIVERSITY OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

GvHD; humanized mice; immune reconstitution; IVIG

Indexed keywords

CYCLOSPORIN A; GAMMA INTERFERON; IMMUNOGLOBULIN; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 2; OKT 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE ASSOCIATION; DRUG USE; GRAFT VERSUS HOST REACTION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOSTIMULATION; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; RISK REDUCTION; SURVIVAL RATE; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD34; CELL PROLIFERATION; CELL TRANSPLANTATION; CYTOKINES; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; GRAFT VS HOST DISEASE; HUMANS; IMMUNE SYSTEM; IMMUNOGLOBULINS; INTERFERON-GAMMA; INTERLEUKIN-15; INTERLEUKIN-17; INTERLEUKIN-2; MICE; MICE, INBRED NOD; MICE, SCID; T-LYMPHOCYTES;

EID: 84858069440     PISSN: 02683369     EISSN: 14765365     Source Type: Journal    
DOI: 10.1038/bmt.2011.93     Document Type: Article

References (78)

1. Ferrara JL, Cooke KR, Pan L, Krenger W. The immunopathophysiology of acute graft-versus-host-disease. Stem Cells 1996; 14: 473-489. (Pubitemid 26322109)
2. Ferrara JL, Cooke KR, Teshima T. The pathophysiology of acute graft-versus-host disease. Int J Hematol 2003; 78: 181-187. (Pubitemid 37288503)
3. Ferrara JL, Deeg HJ. Graft-versus-host disease. N Engl J Med 1991; 324: 667-674.
4. Goker H, Haznedaroglu IC, Chao NJ. Acute graft-vs-host disease: pathobiology and management. Exp Hematol 2001; 29: 259-277. (Pubitemid 32223460)
5. Lazarus HM, Coccia PF, Herzig RH, Graham-Pole J, Gross S, Strandjord S et al. Incidence of acute graft-versus-host disease with and without methotrexate prophylaxis in allogeneic bone marrow transplant patients. Blood 1984; 64: 215-220. (Pubitemid 14083878)
6. Sullivan KM, Deeg HJ, Sanders J, Klosterman A, Amos D, Shulman H et al. Hyperacute graft-v-host disease in patients not given immunosuppression after allogeneic marrow transplantation. Blood 1986; 67: 1172-1175. (Pubitemid 16116437)
7. Chao NJ. Graft-vs-Host Disease, 2nd edn. Landes Bioscience: Austin, 1999.
8. Balduzzi A, Gooley T, Anasetti C, Sanders JE, Martin PJ, Petersdorf EW et al. Unrelated donor marrow transplantation in children. Blood 1995; 86: 3247-3256.
9. Martin PJ. Increased disparity for minor histocompatibility antigens as a potential cause of increased GVHD risk in marrow transplantation from unrelated donors compared with related donors. Bone Marrow Transplant 1991; 8: 217-223.
10. Anasetti C, Beatty PG, Storb R, Martin PJ, Mori M, Sanders JE et al. Effect of HLA incompatibility on graft-versus-host disease, relapse, and survival after marrow transplantation for patients with leukemia or lymphoma. Hum Immunol 1990; 29: 79-91. (Pubitemid 20357658)
11. Negi VS, Elluru S, Siberil S, Graff-Dubois S, Mouthon L, Kazatchkine MD et al. Intravenous immunoglobulin: an update on the clinical use and mechanisms of action. J Clin Immunol 2007; 27: 233-245. (Pubitemid 46790823)
12. Sokos DR, Berger M, Lazarus HM. Intravenous immunoglobulin: appropriate indications and uses in hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 2002; 8: 117-130. (Pubitemid 34285070)
13. Sullivan KM, Kopecky KJ, Jocom J, Fisher L, Buckner CD, Meyers JD et al. Immunomodulatory and antimicrobial efficacy of intravenous immunoglobulin in bone marrow transplantation. N Engl J Med 1990; 323: 705-712. (Pubitemid 20288939)
14. Cordonnier C, Chevret S, Legrand M, Rafi H, Dhedin N, Lehmann B et al. Should immunoglobulin therapy be used in allogeneic stem-cell transplantation? A randomized, double-blind, dose effect, placebo-controlled, multicenter trial. Ann Intern Med 2003; 139: 8-18.
15. Feinstein LC, Seidel K, Jocum J, Bowden RA, Anasetti C, Deeg HJ et al. Reduced dose intravenous immunoglobulin does not decrease transplant-related complications in adults given related donor marrow allografts. Biol Blood Marrow Transplant 1999; 5: 369-378.
16. Klaesson S, Ringden O, Ljungman P, Aschan J, Hagglund H, Winiarski J. Does high-dose intravenous immune globulin treatment after bone marrow transplantation increase mortality in veno-occlusive disease of the liver? Transplantation 1995; 60: 1225-1230. (Pubitemid 26005276)
17. Sullivan KM, Storek J, Kopecky KJ, Jocom J, Longton G, Flowers M et al. A controlled trial of long-term administration of intravenous immunoglobulin to prevent late infection and chronic graft-vs-host disease after marrow transplantation: clinical outcome and effect on subsequent immune recovery. Biol Blood Marrow Transplant 1996; 2: 44-53. (Pubitemid 126488195)
18. Winston DJ, Antin JH, Wolff SN, Bierer BE, Small T, Miller KB et al. A multicenter, randomized, double-blind comparison of different doses of intravenous immunoglobulin for prevention of graft-versus-host disease and infection after allogeneic bone marrow transplantation. Bone Marrow Transplant 2001; 28: 187-196. (Pubitemid 32725720)
19. Shultz LD, Lyons BL, Burzenski LM, Gott B, Chen X, Chaleff S et al. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J Immunol 2005; 174: 6477-6489. (Pubitemid 40663843)
20. Gan R, Yin Z, Liu T, Wang L, Tang Y, Song Y. Cyclosporine A effectively inhibits graft-versus-host disease during development of Epstein-Barr virus-infected human B cell lymphoma in SCID mouse. Cancer Sci 2003; 94: 796-801. (Pubitemid 37258778)
21. Roychowdhury S, Blaser BW, Freud AG, Katz K, Bhatt D, Ferketich AK et al. IL-15 but not IL-2 rapidly induces lethal xenogeneic graft-versus-host disease. Blood 2005; 106: 2433-2435. (Pubitemid 41510817)
22. Cooke KR, Kobzik L, Martin TR, Brewer J, Delmonte Jr J, Crawford JM et al. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood 1996; 88: 3230-3239. (Pubitemid 26357409)
23. Siragam V, Crow AR, Brinc D, Song S, Freedman J, Lazarus AH. Intravenous immunoglobulin ameliorates ITP via activating Fc gamma receptors on dendritic cells. Nat Med 2006; 12: 688-692. (Pubitemid 43865239)
24. Aubin E, Lemieux R, Bazin R. Indirect inhibition of in vivo and in vitro T-cell responses by intravenous immunoglobulins due to impaired antigen presentation. Blood 2010; 115: 1727-1734.
25. Ito R, Katano I, Kawai K, Hirata H, Ogura T, Kamisako T et al. Highly sensitive model for xenogenic GVHD using severe immunodeficient NOG mice. Transplantation 2009; 87: 1654-1658.
26. King MA, Covassin L, Brehm MA, Racki W, Pearson T, Leif J et al. Human peripheral blood leucocyte non-obese diabetic-severe combined immunodeficiency interleukin-2 receptor gamma chain gene mouse model of xenogeneic graft-versus-host-like disease and the role of host major histocompatibility complex. Clin Exp Immunol 2009; 157: 104-118.
27. Locatelli F, Bruno B, ZeccaM, Van-LintMT, McCann S, Arcese W et al. Cyclosporin A and short-term methotrexate versus cyclosporin A as graft versus host disease prophylaxis in patients with severe aplastic anemia given allogeneic bone marrow transplantation from an HLA-identical sibling: results of a GITMO/EBMT randomized trial. Blood 2000; 96: 1690-1697. (Pubitemid 30661050)
28. Locatelli F, Zecca M, Rondelli R, Bonetti F, Dini G, Prete A et al. Graft versus host disease prophylaxis with low-dose cyclosporine-A reduces the risk of relapse in children with acute leukemia given HLA-identical sibling bone marrow transplantation: results of a randomized trial. Blood 2000; 95: 1572-1579. (Pubitemid 30120815)
29. Olsson R, Remberger M, Hassan Z, Omazic B, Mattsson J, Ringden O. GVHD prophylaxis using low-dose cyclosporine improves survival in leukaemic recipients of HLA-identical sibling transplants. Eur J Haematol 2010; 84: 323-331.
30. Storb R, Deeg HJ, Farewell V, Doney K, Appelbaum F, Beatty P et al. Marrow transplantation for severe aplastic anemia: methotrexate alone compared with a combination of methotrexate and cyclosporine for prevention of acute graft-versus-host disease. Blood 1986; 68: 119-125. (Pubitemid 16041720)
31. Gratama JW, Jansen J, Lipovich RA, Tanke HJ, Goldstein G, Zwaan FE. Treatment of acute graft-versus-host disease with monoclonal antibody OKT3. Clinical results and effect on circulating T lymphocytes. Transplantation 1984; 38: 469-474. (Pubitemid 15207399)
32. Knop S, Hebart H, Gscheidle H, Holler E, Kolb HJ, Niederwieser D et al. OKT3 muromonab as second-line and subsequent treatment in recipients of stem cell allografts with steroid-resistant acute graft-versus-host disease. Bone Marrow Transplant 2005; 36: 831-837. (Pubitemid 41613308)
33. Gleixner B, Kolb HJ, Holler E, Liesenfeld S, Riedner C, Hiller E et al. Treatment of aGVHD with OKT3: clinical outcome and side-effects associated with release of TNF alpha. Bone Marrow Transplant 1991; 8: 93-98.
34. Martin PJ, Hansen JA, Anasetti C, Zutter M, Durnam D, Storb R et al. Treatment of acute graft-versus-host disease with anti-CD3 monoclonal antibodies. Am J Kidney Dis 1988; 11: 149-152. (Pubitemid 18072902)
35. Hebart H, Ehninger G, Schmidt H, Berner B, Reuss-Borst M, Waller HD et al. Treatment of steroid-resistant graft-versus-host disease after allogeneic bone marrow transplantation with anti-CD3/TCR monoclonal antibodies. Bone Marrow Transplant 1995; 15: 891-894.
36. Benekli M, Hahn T, Williams BT, Cooper M, Roy HN, Wallace P et al. Muromonab-CD3 (Orthoclone OKT3), methylprednisolone and cyclosporine for acute graft-versus-host disease prophylaxis in allogeneic bone marrow transplantation. Bone Marrow Transplant 2006; 38: 365-370.
37. Cantoni N, Weisser M, Buser A, Arber C, Stern M, Heim D et al. Infection prevention strategies in a stem cell transplant unit: impact of change of care in isolation practice and routine use of high dose intravenous immunoglobulins on infectious complications and transplant related mortality. Eur J Haematol 2009; 83: 130-138.
38. Tha-In T, Bayry J, Metselaar HJ, Kaveri SV, Kwekkeboom J. Modulation of the cellular immune system by intravenous immunoglobulin. Trends Immunol 2008; 29: 608-615.
39. Kessel A, Ammuri H, Peri R, Pavlotzky ER, Blank M, Shoenfeld Y et al. Intravenous immunoglobulin therapy affects T regulatory cells by increasing their suppressive function. J Immunol 2007; 179: 5571-5575.
40. Anthony RM, Nimmerjahn F, Ashline DJ, Reinhold VN, Paulson JC, Ravetch JV. Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc. Science 2008; 320: 373-376. (Pubitemid 351555659)
41. Anthony RM, Wermeling F, Karlsson MC, Ravetch JV. Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc Natl Acad Sci USA 2008; 105: 19571-19578.
42. Tha-In T, Metselaar HJ, Tilanus HW, Boor PP, Mancham S, Kuipers EJ et al. Superior immunomodulatory effects of intravenous immunoglobulins on human T-cells and dendritic cells: comparison to calcineurin inhibitors. Transplantation 2006; 81: 1725-1734. (Pubitemid 43948307)
43. Tha-In T, Metselaar HJ, Tilanus HW, Groothuismink ZM, Kuipers EJ, de Man RA et al. Intravenous immunoglobulins suppress T-cell priming by modulating the bidirectional interaction between dendritic cells and natural killer cells. Blood 2007; 110: 3253-3262. (Pubitemid 350106318)
44. Cottler-Fox M, Lynch M, Pickle LW, Cahill R, Spitzer TR, Deeg HJ. Some but not all benefits of intravenous immunoglobulin therapy after marrow transplantation appear to correlate with IgG trough levels. Bone Marrow Transplant 1991; 8: 27-33.
45. Abdel-Mageed A, Graham-Pole J, Del Rosario ML, Longmate J, Ochoa S, Amylon M et al. Comparison of two doses of intravenous immunoglobulin after allogeneic bone marrow transplants. Bone Marrow Transplant 1999; 23: 929-932. (Pubitemid 29213696)
46. Halloran PF, Helms LM, Kung L, Noujaim J. The temporal profile of calcineurin inhibition by cyclosporine in vivo. Transplantation 1999; 68: 1356-1361.
47. Rao A. NF-ATp: a transcription factor required for the coordinate induction of several cytokine genes. Immunol Today 1994; 15: 274-281. (Pubitemid 24170521)
48. Jain J, Loh C, Rao A. Transcriptional regulation of the IL-2 gene. Curr Opin Immunol 1995; 7: 333-342.
49. Serfling E, Avots A, Neumann M. The architecture of the interleukin-2 promoter: a reflection of T lymphocyte activation. Biochim Biophys Acta 1995; 1263: 181-200.
50. Podtschaske M, Benary U, Zwinger S, Hofer T, Radbruch A, Baumgrass R. Digital NFATc2 activation per cell transforms graded T cell receptor activation into an all-or-none IL-2 expression. PLoS One 2007; 2: e935.
51. Cosimi AB. Clinical development of Orthoclone OKT3. Transplant Proc 1987; 19(Suppl 1): 7-16. (Pubitemid 17068056)
52. Pinana JL, Valcarcel D, Fernandez-Aviles F, Martino R, Rovira M, Barba P et al. MTX or mycophenolate mofetil with CsA as GVHD prophylaxis after reduced-intensity conditioning PBSCT from HLA-identical siblings. Bone Marrow Transplant 2010; 45: 1449-1456.
53. Amran D, Renz H, Lack G, Bradley K, Gelfand EW. Suppression of cytokine-dependent human T-cell proliferation by intravenous immunoglobulin. Clin Immunol Immunopathol 1994; 73: 180-186. (Pubitemid 24335398)
54. Andersson J, Skansen-Saphir U, Sparrelid E, Andersson U. Intravenous immune globulin affects cytokine production in T lymphocytes and monocytes/macrophages. Clin Exp Immunol 1996; 104(Suppl 1): 10-20.
55. Modiano JF, Amran D, Lack G, Bradley K, Ball C, Domenico J et al. Posttranscriptional regulation of T-cell IL-2 production by human pooled immunoglobin. Clin Immunol Immunopathol 1997; 83: 77-85. (Pubitemid 27128399)
56. MacMillan HF, Lee T, Issekutz AC. Intravenous immunoglobulin G-mediated inhibition of T-cell proliferation reflects an endogenous mechanism by which IgG modulates T-cell activation. Clin Immunol 2009; 132: 222-233.
57. Aktas O, Waiczies S, Grieger U, Wendling U, Zschenderlein R, Zipp F. Polyspecific immunoglobulins (IVIg) suppress proliferation of human (auto)antigen-specific T cells without inducing apoptosis. J Neuroimmunol 2001; 114: 160-167. (Pubitemid 32184737)
58. Ephrem A, Chamat S, Miquel C, Fisson S, Mouthon L, Caligiuri G et al. Expansion of CD4+CD25+ regulatory T cells by intravenous immunoglobulin: a critical factor in controlling experimental autoimmune encephalomyelitis. Blood 2008; 111: 715-722.
59. Achiron A, Margalit R, Hershkoviz R, Markovits D, Reshef T, Melamed E et al. Intravenous immunoglobulin treatment of experimental T cell-mediated autoimmune disease. Upregulation of T cell proliferation and downregulation of tumor necrosis factor alpha secretion. J Clin Invest 1994; 93: 600-605.
60. Zhang C, Zhang J, Yang B, Wu C. Cyclosporin A inhibits the production of IL-17 by memory Th17 cells from healthy individuals and patients with rheumatoid arthritis. Cytokine 2008; 42: 345-352.
61. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001; 19: 683-765. (Pubitemid 32368050)
62. Brandt C, Liman P, Bendfeldt H, Mueller K, Reinke P, Radbruch A et al. Whole blood flow cytometric measurement of NFATc1 and IL-2 expression to analyze cyclosporine A-mediated effects in T cells. Cytometry A 2010; 77: 607-613.
63. Yi T, Zhao D, Lin CL, Zhang C, Chen Y, Todorov I et al. Absence of donor Th17 leads to augmented Th1 differentiation and exacerbated acute graft-versus-host disease. Blood 2008; 112: 2101-2110.
64. Chen X, Vodanovic-Jankovic S, Johnson B, Keller M, Komorowski R, Drobyski WR. Absence of regulatory T-cell control of TH1 and TH17 cells is responsible for the autoimmune-mediated pathology in chronic graft-versus-host disease. Blood 2007; 110: 3804-3813. (Pubitemid 350159652)
65. Kappel LW, Goldberg GL, King CG, Suh DY, Smith OM, Ligh C et al. IL-17 contributes to CD4-mediated graft-versus-host disease. Blood 2009; 113: 945-952.
66. Carlson MJ, West ML, Coghill JM, Panoskaltsis-Mortari A, Blazar BR, Serody JS. In vitro-differentiated TH17 cells mediate lethal acute graft-versus-host disease with severe cutaneous and pulmonary pathologic manifestations. Blood 2009; 113: 1365-1374.
67. Iclozan C, Yu Y, Liu C, Liang Y, Yi T, Anasetti C et al. T helper17 cells are sufficient but not necessary to induce acute graft-versus-host disease. Biol Blood Marrow Transplant 2010; 16: 170-178.
68. Tournadre A, Lenief V, Miossec P. Expression of TLR3 and TLR7 in muscle is characteristic of inflammatory myopathy and is differentially regulated by Th1 and Th17 cytokines. Arthritis Rheum 2010; 62: 2144-2151.
69. Giraud P, Thuret I, Reviron D, Chambost H, Brunet C, Novakovitch G et al. Immune reconstitution and outcome after unrelated cord blood transplantation: a single paediatric institution experience. Bone Marrow Transplant 2000; 25: 53-57. (Pubitemid 30093156)
70. Niehues T, Rocha V, Filipovich AH, Chan KW, Porcher R, Michel G et al. Factors affecting lymphocyte subset reconstitution after either related or unrelated cord blood transplantation in children-a Eurocord analysis. Br J Haematol 2001; 114: 42-48. (Pubitemid 32702631)
71. Talvensaari K, Clave E, Douay C, Rabian C, Garderet L, Busson M et al. A broad T-cell repertoire diversity and an efficient thymic function indicate a favorable long-term immune reconstitution after cord blood stem cell transplantation. Blood 2002; 99: 1458-1464. (Pubitemid 34547105)
72. Thomson BG, Robertson KA, Gowan D, Heilman D, Broxmeyer HE, Emanuel D et al. Analysis of engraftment, graft-versus-host disease, and immune recovery following unrelated donor cord blood transplantation. Blood 2000; 96: 2703-2711.
73. Hiramatsu H, Nishikomori R, Heike T, Ito M, Kobayashi K, Katamura K et al. Complete reconstitution of human lymphocytes from cord blood CD34+ cells using the NOD/SCID/gammacnull mice model. Blood 2003; 102: 873-880. (Pubitemid 36917778)
74. Rajesh D, Zhou Y, Jankowska-Gan E, Roenneburg DA, Dart ML, Torrealba J et al. Th1 and Th17 immunocompetence in humanized NOD/SCID/IL2rgammanull mice. Hum Immunol 2010; 71: 551-559.
75. Yahata T, Ando K, Nakamura Y, Ueyama Y, Shimamura K, Tamaoki N et al. Functional human T lymphocyte development from cord blood CD34+ cells in nonobese diabetic/Shi-scid, IL-2 receptor gamma null mice. J Immunol 2002; 169: 204-209. (Pubitemid 34686137)
76. Ishikawa F, Yasukawa M, Lyons B, Yoshida S, Miyamoto T, Yoshimoto G et al. Development of functional human blood and immune systems in NOD/SCID/IL2 receptor {gamma} chain(null) mice. Blood 2005; 106: 1565-1573. (Pubitemid 41208567)
77. Watanabe S, Terashima K, Ohta S, Horibata S, Yajima M, Shiozawa Y et al. Hematopoietic stem cell-engrafted NOD/ SCID/IL2Rgamma null mice develop human lymphoid systems and induce long-lasting HIV-1 infection with specific humoral immune responses. Blood 2007; 109: 212-218. (Pubitemid 46070123)
78. Seite JF, Cornec D, Renaudineau Y, Youinou P, Mageed RA, Hillion S. IVIg modulates BCR-signaling through CD22 and promotes apoptosis in mature human B lymphocytes. Blood 2010; 116: 1698-1704.